Abstract

How ecological and evolutionary processes interact and together determine species and community responses to climate change is poorly understood. We studied long-term dynamics (over approximate-ly 200 asexual generations) in two phytoplankton species, a coccolithophore (Emiliania huxleyi) and a diatom (Chaetoceros affinis), to increased CO2 growing alone or competing with one another in co-occurrence. To allow for rapid evolutionary responses, the experiment started with a standing genetic variation of nine genotypes in each of the species. Under co-occurrence of both species, we observed a dominance shift from C. affinis to E. huxleyi after about 120 generations in both CO2 treatments, but more pronounced under high CO2. Associated with this shift, we only found weak adaptation to high CO2 in the diatom and none in the coccolithophore in terms of species´ growth rates. In addition, no adaptation to interspecific competition could be observed by comparing the single to the two-species treatments in reciprocal assays, regardless of the CO2 treatment. Nevertheless, highly reproducible genotype sorting left only one genotype remaining for each of the species among all treatments. This strong evolutionary selection coincided with the dominance shift from C. affinis to E. huxleyi. Since all other conditions were kept constant over time, the most parsimonious explanation for the dominance shift is that the strong evolutionary selection was driven by the experimental nutrient conditions, and in turn potentially altered competitive ability of the two species. Thus, here observed changes in the simplest possible two-species phytoplankton "community" demonstrated that eco-evolutionary interactions can be critical for predicting community responses to climate change in rapidly dividing organisms such as phytoplankton.

Highlights

  • Recent studies have repeatedly shown that ecological and evolutionary processes happen on similar time scales (Carroll et al, 2007; Reznick, 2013)

  • From ca. 160 days onward there was a dominance reversal from C. affinis to E. huxleyi (Figure 2 and Supplementary Table S4 Full Model “Time” F1,337 = 613.093, p < 0.0001,“Selection CO2 × Time” F1,337 = 26.036, and p < 0.0001), and a different reaction of both species to CO2, with E. huxleyi being favored by high CO2 in the second phase of the experiment

  • Similar to the dynamics of relative species contributions, the time course of absolute biovolume of both species was characterized by two distinct phases that changed around 160 days of the experiment (Figures 3A–D and Supplementary Table S5 E. huxleyi and C. affinis single and interactive effects of “Time” in Full model)

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Summary

Introduction

Recent studies have repeatedly shown that ecological and evolutionary processes happen on similar time scales (Carroll et al, 2007; Reznick, 2013). With one cell division per day, many species lend themselves for experimental studies allowing for appropriate replication and hundreds of generations of evolutionary change (Reusch and Boyd, 2013) Their ecological importance cannot be overemphasized, as marine phytoplankton species are responsible for half of all global photosynthesis (Falkowski et al, 2008). On time scales too short for evolutionary adaptation, non-calcifying species mostly respond by enhanced growth (Schaum et al, 2012; Li et al, 2017) leading to higher abundances (Sommer et al, 2015; “ecological winners,” e.g., diatoms), while most calcifying species react negatively (“ecological losers,” e.g., coccolithophores) to CO2 enrichment (Riebesell, 2004; Doney et al, 2009). Nested within such broad functional categories of sensitivity is pronounced intraspecific variation (Schaum et al, 2012; Hattich et al, 2017; Des Roches et al, 2018), on which selection can operate (Lohbeck et al, 2012)

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